E3S Web of Conferences 1, 34004 (2013) DOI: 10.1051/e3sconf/20130134004 C Owned by the authors, published by EDP Sciences, 2013

Polonium 210Po, uranium (234U, 238U) and plutonium (238Pu, 239+240Pu) bioaccumulation in marine birds

D. I. Strumińska-Parulska1, A. Boryło1, B. Skwarzec1 and J. Fabisiak2

1 University of Gdańsk, Faculty of Chemistry, Sobieskiego 18/19, 80-952 Gdańsk, Poland, [email protected] 2 Naval Academy, Śmidowicza 61, 81-103 Gdynia, Poland

Abstract. The aim of this work was the determination of 210Po, 234U, 238U, 238Pu and 239+240Pu concentration in marine birds which permanently or temporally live in the southern Baltic Sea coast. We chose 11 species of seabirds: three species permanently residing at southern Baltic Sea, four species of wintering birds and three species of migrating birds. The results show that analyzed radionuclides are non-uniformly distributed in the marine birds. The highest activities of 210Po were observed in feathers, muscles and liver. The highest uranium content was found in liver, rest of viscera and feathers, while plutonium in the digestion organs and feathers. Omnivore seabirds accumulated more polonium, plutonium than species that feed on fish, while herbivore seabirds accumulated more uranium than carnivore.

Keywords: polonium, uranium, plutonium, marine birds, bioaccumulation, Baltic Sea

Introduction

The estimation of the size of contamination caused by radioactive). Various components of uranium can alpha radioactive elements in the natural environment penetrate the blood from alveolus pockets in the lungs or and their effects on living organisms is one of the most through the gastrointestinal tract. The presence of uranium important issues of the radiochemical and radiological in the body can cause damage to the kidney, leading to protection. Among alpha radioactive elements present in nephritis (Tutu et al., 2005). Most of uranium in the the environment, polonium plays an important role environment is located in terrigenic materials (Skwarzec because 210Po belongs to the most radiotoxic nuclides to et al., 2006). Natural uranium concentration in rivers human beings. The most important natural source of varies linearly with salinity (Skwarzec, 1995). Man-made 210Po in the environment is uranium decay series starting plutonium is widespread all over the world, takes part in from 238U. Polonium is strongly accumulated in the geochemical circulation and accumulates in the food marine biota and for this reason it is an important source chain. The main source of plutonium in Poland and the of radiation dose in the body of marine animals Baltic Sea, before the Chernobyl accident, was global (Skwarzec, 1995). The intensive studies on the fallout from nuclear weapons testing. Other sources of occurrence and distribution of 210Po in the ecosystem of plutonium, e.g. releases from the spent fuel facilities at the southern Baltic help to recognize mechanisms and Sellafield (UK) and Cap de la Hague (France), are less circulation of polonium in the environment. Uranium important (Skwarzec, 1995; Strumińska-Parulska and occurs naturally in the Earth’s crust and occurs in much Skwarzec, 2010). Plutonium can be accumulated in the higher concentrations, along with thorium and rare earth marine biota and for this reason it is an important source element in the area where monazite sand prevails of radiation dose in the body of marine animals 239+240 (Skwarzec, 1995). The average concentration of uranium (Skwarzec,1995). The total Pu amount in the Baltic in the Earth’s crust is 410-4%. The isotope 238U is the Sea was estimated at 15.2-24.2 TBq and over 90% is parent nuclide of the radioactive decay uranium-radium deposited in sediments, about 0.2 TBq exists in water and series. Uranium is relatively highly toxic to human, both only a few GBq is accumulated in biota (Salo et al., 1986). chemically and radiologically (its progeny are highly Birds are characterized by high body temperature and intensive metabolism what cause high daily food

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Article available at http://www.e3s-conferences.org or http://dx.doi.org/10.1051/e3sconf/20130134004 E3S Web of Conferences requirement (Tomiałojć and Stawarczyk, 2003). Most of in Tab. 1. The data show that 210Po is non-uniformly them are double-environment animals. That is why they distributed in tissues and organs of the seabirds. The are an important part of the ecosystems. Seabirds are a highest 210Po concentrations were mostly in liver and very important element of the trophic chain of marine ranged from 0.16 Bq kg-1 ww in tufted duck to 18.90 Bq ecosystem. Particularly the birds’ feathers are often used kg-1 ww in long-tailed duck. The high 210Po concentrations as a bioindicator of metal contamination of marine and were also observed in feathers and ranged from 0.47 Bq air environment (Burger and Gochfeld, 1997). kg-1 ww in tufted duck to 5.70 Bq kg-1 ww in great Knowledge on the polonium, uranium and plutonium cormorant. Among the analyzed species of sea birds, the distribution in birds is very poor. From over 9000 highest 210Po concentration in whole organism was species of birds in the world, 438 species have been measured in long-tailed duck at 3.54 Bq kg-1 ww (Tab. 1). registered in Poland, of which 230 birds live in the The 210Po concentration in tissues and organs of this bird Polish area of the Baltic Sea (Tomiałojć and Stawarczyk, was much higher than in the rest of the analyzed species 2003). The aim of this work was determination of 210Po, of sea birds. The analysis of diet and feeding habit showed 234U, 238U, 238Pu and 239+240Pu concentration in marine that it is a very important aspect of 210Po accumulation in birds from the southern Baltic Sea coast as well as tissues and organs of sea birds from the southern Baltic recognition of their accumulation in different organs and Sea. The 210Po concentration was higher in omnivore tissues analyzed birds. Moreover, the studies can help to marine birds as as long-tailed duck, velvet scoter, black recognize the radionuclides sources in marine birds as guillemot and eurasian coot feeding on crustaceans, well as their connection with their diet and living habits. mollusks, fish, plants and algae. The 210Po concentration was lower in tissues and organs of predatory fish-feeding Material and Methods seabirds as great cormorant and common guillemot or herbivore birds as tufted duck. The results of our studies Among bird species registered in the Polish area of the show that the 210Po concentration was higher in wintering southern Baltic Sea, there are three main groups: sea sea birds such as long-tailed duck, black guillemot and birds which permanently reside, principally in Gdansk velvet scoter. The differences in accumulation of trace Bay and Puck Bay, wintering birds and migratory birds. elements in birds are also connected with diet and place of The following sea birds were collected for research: 1. residence (Skwarzec and Fabisiak, 2007). seabirds which permanently reside in the southern Baltic Sea - tufted duck (Aythya fuligula), eurasian coot (Fulica 234U and 238U atra), great cormorant (Phalacrocorax carbo); 2. wintering birds - common eider (Somateria mollissima), The results of 234U and 238U concentration as well as total velvet scoter (Melanitta fusca), black guillemot uranium concentration in organs and tissues of analyzed (Cepphus grylle), long-tailed duck (Clangula hyemalis), marine birds were presented in Table 1. The obtained 3. migratory birds - razorbill (Alca torda), common results indicated that uranium is non-uniformly distributed guillemot (Uria aalge), red-throated diver (Gavia in tissues and organs of analyzed marine birds. The stellata) (Skwarzec and Fabisiak, 2007; Boryło et al., highest values of 234U and 238U were measured in rest of 2010; Strumińska-Parulska et al., 2011). The fresh viscera: from 46.6 and 48.3 mBq kg-1 ww in razorbill to samples were weighted, homogenized and digested using 919 and 921 mBq kg-1 ww in tufted duck and in feathers 209 232 -1 65% HNO3 with a Po (50 mBq), U (32.5 mBq) and as well: from 68.7 and 76.7 mBq kg ww in eurasian coot 242Pu (5 mBq) spikes added as a yield tracers. The to 341 and 294 mBq kg-1 ww in great cormorant. Further radiochemical method allows Po, U and Pu studies showed the maximum uranium concentrations determination from the same sample (Skwarzec, 1995, were found in herbivorous as eurasian coot and tufted Skwarzec and Fabisiak, 2007; Skwarzec, 2009, Boryło et duck while lower were estimated for predatory as razorbill al., 2010; Strumińska-Parulska et al., 2011). After and great cormorant. (Tab. 1). Food is a very important radiochemical preparation, the activities of 210Po, 234U, source of uranium in marine birds. The uranium 238U, 238Pu and 239+240Pu radionuclides were measured concentration was higher for visitant birds in region of the separately using alpha spectrometer (Alpha Analyst, Gulf of Gdańsk in period from October to April (tufted Canberra Packard) equipped with PIPS detectors. The duck and eurasian coot). On account of birds moulting, we accuracy and precision of the radiochemical method observed higher uranium concentration for species, which were evaluated using IAEA reference materials and permanently live on the land (great cormorant, common estimated at less than 7%. eider, eurasian coot). The obtained results are in agreement to values Results and Discussion reported for marine organisms in southern Baltic Sea

210 (Skwarzec, 1995). Bioaccumulation of uranium by marine Po birds is slight, because his radionuclide is quickly removed from organism. The results of 210Po concentration in tissues and organs of marine birds from the southern Baltic Sea are shown

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Tab.1 Polonium 210Po, uranium 234U and 238U and plutonium 238 Pu and 239+240Pu concentrations in organs and tissues of analyzed seabirds (Skwarzec and Fabisiak, 2007; Boryło et al., 2010; Strumińska-Parulska et al., 2011) Concentration Organ, 210Po 234U 238U 238Pu 239+240Pu 210Po 234U 238U 238Pu 239+240Pu tissue -1 -1 [Bq kg ww] [mBq kg-1 ww] [mBq kg-1 ww] [Bq kg ww] [mBq kg-1 ww] [mBq kg-1 ww] Great cormorant (Phalacrocorax carbo) (n=1) Eurasian coot (Fulica atra) (n=1) Liver 0.29 15.7 16.29 0.28 2.21 - - - - - Muscle 0.05 3.35 3.45 0.06 0.19 0.34 42.5 41.9 0.17 0.34 Feathers 5.70 341 294 0.10 0.37 2.99 68.7 76.7 0.15 0.52 Skeleton 0.22 10.4 11.3 0.02 0.05 3.38 40.5 41.7 0.05 0.42 Skin 0.35 76.9 65.6 0.03 0.13 0.49 35.5 37.0 0.10 0.52 Viscera 0.32 66.6 63.4 0.06 0.25 2.57 395 409 0.18 2.07 Body 0.59 50.0 44.6 0.05 0.22 2.10 134 139 0.13 0.84 Razorbill (Alca torda) (n=9) Tufted duck (Aythya fuligula) (n=2) Liver 3.86 57.2 58.2 0.71 1.28 0.16 66.9 91.1 1.64 2.86 Muscle 0.99 2.71 2.56 0.38 0.82 0.05 11.5 10.6 0.12 0.24 Feathers 2.81 116 101 0.29 2.78 0.47 98.6 96.3 0.32 0.89 Skeleton 0.59 15.4 12.5 0.50 1.55 1.24 63.0 63.0 - - Skin 0.66 19.1 17.0 0.29 1.36 0.10 30.6 30.2 0.23 0.39 Viscera 1.43 46.6 48.3 0.52 1.12 1.48 919 921 0.15 1.66 Body 1.22 31.4 28.5 0.41 1.44 0.69 220 221 - - Common eider (Somateria mollissima) (n=13) Long-tailed duck (Clangula hyemalis) (n=13) Liver 2.92 9.42 9.04 0.18 0.48 18.90 14.4 14.0 0.38 1.52 Muscle 1.24 7.80 7.00 0.05 0.48 2.30 11.6 10.1 0.40 0.80 Feathers 2.78 259 232 0.29 2.87 2.59 168 156 0.24 1.35 Skeleton 0.51 138 126 0.52 1.86 1.98 42.7 39.5 0.65 4.31 Skin 0.83 47.1 42.0 0.04 0.11 5.16 63.6 60.2 0.37 1.49 Viscera 0.82 293 260 0.05 1.22 2.59 89.0 84.7 0.05 1.46 Body 1.15 127 113 0.20 1.16 3.54 60.5 56.5 0.31 2.10 Velvet scoter (Melanitta fusca) (n=12) Black guillemot (Cepphus gryle) (n=2) Liver 4.62 11.9 17.2 0.15 0.65 6.30 25.9 32.4 0.42 1.70 Muscle 0.73 6.8 7.07 0.53 1.44 1.54 50.3 144 0.04 0.40 Feathers 3.72 83.0 78.5 - - 4.05 271 279 0.24 3.40 Skeleton 3.17 12.3 11.3 0.10 0.59 1.89 30.3 41.9 0.08 0.40 Skin 0.82 40.7 38.3 0.08 0.80 0.41 62.9 61.4 0.26 0.47 Viscera 1.36 130 118 1.81 4.0 1.96 55.4 54.3 0.50 4.25 Body 2.00 42.1 39.4 - - 2.13 75.7 100 0.20 1.36 Red-throated diver (Govia stellata) (n=7) Common guillemot (Uria aalge) (n=2)

Liver 3.67 4.21 4.02 0.43 0.79 1.23 83.1 88.8 0.23 1.38 Muscle 0.31 4.52 4.17 0.19 0.48 0.07 4.20 5.60 0.12 0.23 Feathers 1.05 140 122 0.22 1.76 2.92 157 136 0.40 1.24 Skeleton 0.42 9.85 7.85 0.19 1.69 0.57 10.4 11.1 0.19 0.38 Skin 0.33 33.0 28.3 0.52 1.11 0.15 24.4 23.9 0.10 0.30 Viscera 1.56 127 125 0.45 1.22 0.31 56.1 102 0.34 0.68 Body 0.74 43.2 39.3 0.30 1.16 0.59 32.6 34.4 0.18 0.47

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238Pu and 239+240Pu References All results of 238Pu and 239+240Pu plutonium concentrations are presented in Table 1. The obtained results indicated Boryło A, Skwarzec J, Fabisiak J. Bioaccumulation of that the plutonium is non-uniformly distributed in organs uranium 234U and 238U in marine birds. J Radioanal and tissues of analyzed seabirds. Generally the highest Nucl Chem 2010;284:165. plutonium concentrations were found in the digestion Burger, J, Gochfeld, M. Risk, mercury levels, and birds: organs, skeleton and feathers. Among analyzed birds the relating adverse laboratory effects to field highest 239+240Pu concentration was found in skeleton, its biomonitoring. Environ Res. 1997;75:160. activities in this tissue ranged from 0.05 mBq kg-1 ww in Salo A, Toumainen K, Voipio A. Inventories of certain great cormorant to 4.31 mBq kg-1 ww in long-tail duck long-lived radionuclides in the Baltic Sea. In: Study (Tab. 1). The concentrations of 239+240Pu in seabirds are of Radioactive Materials in the Baltic Sea. IAEA- lower in comparison to fish from the southern Baltic Sea TECDOC-362 Vienna; 1986:53. as well as in comparison to phytobenthos, crustaceans and Skwarzec B. Polon, uran i pluton w ekosystemie bivalves (Strumińska-Parulska and Skwarzec, 2010). południowego Bałtyku. 6. Rozprawy i monografie, Generally we observed higher 239+240Pu concentrations in IO PAN. Sopot; 1995. whole body of wintering seabirds (long-tailed duck, black Skwarzec B. Radiochemical methods for the guillemot, common eider) and further in migratory determination of polonium, radiolead, uranium and seabirds (razorbill, common guillemot, red-throated diver). plutonium in environmental samples. Chem Anal These birds had also the highest 239+240Pu concentrations in (Warsaw) 1997;42:107. feathers, viscera and skeleton. Permanently residing in the Skwarzec B. Determination of radionuclides in aquatic southern Baltic Sea seabirds were characterized by the environment. In: Analytical measurement in aquatic highest plutonium concentrations in liver (great cormorant, environments. Tylor&Francis PE 2009: 241. tufted duck). Detailed diet analysis and organs of 239+240Pu Skwarzec B, Strumińska DI, Boryło A. Radionuclides of accumulation allowed for statement that both inhalation iron (55Fe), nickel (63Ni), polonium (210Po), uranium and food play a significant role in its supply. Bird which (234U, 235U, 238U) and plutonium (238Pu, 239+240Pu, eat fish (great cormorant, common guillemot) are 241Pu) in Poland and Baltic Sea environment. characterized by much lower 239+240Pu concentrations in Nukleonika 2006;Suppl.2:45. analyzed organs and tissues similarly as their food - fish Skwarzec B, Fabisiak J. Bioaccumulation of polonium (Skwarzec, 1995). 239+240Pu concentrations in feathers, 210Po in marine birds. J Environ Radioact skeleton and viscera were lower within only fish-eating 2007;93:119. birds (great cormorant, common guillemot) in comparison Strumińska-Parulska DI, Skwarzec B. Plutonium to birds which feed with bivalves, crustaceans or isotopes 238Pu, 239+240Pu, 241Pu and 240Pu/239Pu phytobenthos (eurasian coot, razorbill, black guillemot, atomic ratios in southern Baltic Sea ecosystem. red-throated diver). These results confirm previous Oceanologia 2010;52(3):499. research that fish-eating birds are characterized by lower Strumińska-Parulska DI, Skwarzec B, Fabisiak J. concentrations of radionuclides in comparison to Plutonium bioaccumulation in seabirds. J Environ omnivores (higher concentrations) or plant- and larvae- Radioact 2011;102:1105. eating birds (the highest concentrations). Tomiałojć L, Stawarczyk T. Awifauna Polski. Rozmieszczenie, liczebność i zmiany. PTPP “pro Acknowledgments Natura”. Wrocław 2003. Tutu H, Cukrowska EM, Dohnal V, Havel J. Application The authors would like to thank the Ministry of Science of artificial neural networks for classification of and Higher Education for the financial support under grant uranium distribution in the Central Rand goldfield, DS/8120-4-0176-12. South Africa. Environ Model Assess 2005;10:43.

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